morphological characters and hygienic-sanitary … · morphological characters and...

B. Inst. Pesca, São Paulo, 43(2): 266 - 273, 2017Doi: 10.20950/1678-2305.2017v43n2p266

MORPHOLOGICAL CHARACTERS AND HYGIENIC-SANITARY SIGNIFICANCE OF Tentacularia coryphaenae IN Coryphaena hippurus FROM BRAZIL

Aline Monteiro da SILVA1,2, Sérgio Carmona de SÃO CLEMENTE1, Michelle Cristie Gonçalves da FONSECA2, Delir Corrêa GOMES2, Márcia Cristina Nascimento JUSTO3, Marcelo KNOFF2

Artigo Científico: Recebido em 01/12/2016; Aprovado em 28/05/20171Laboratório de Inspeção e Tecnologia de Pescado, Faculdade de Medicina Veterinária, Universidade Federal Fluminense, Rua Vital Brazil Filho, 64, Vital Brazil, 24320-340 Niterói, RJ, Brasil2Laboratório de Helmintos Parasitos de Vertebrados, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil, 4365, Manguinhos, 21040-900 Rio de Janeiro, RJ, Brasil; e-mail: [email protected] (corresponding author)3Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz, FIOCRUZ, Av. Brasil, 4365, Manguinhos, 21040-900 Rio de Janeiro, RJ, Brasil.

CARACTERES MORFOLÓGICOS E SIGNIFICÂNCIA HIGIÊNICO SANITÁRIA DE Tentacularia coryphaenae EM Coryphaena hippurus DO BRASIL

RESUMOCoryphaena hippurus, ou dourado é uma espécie popular de peixe pescada em torneios de pesca esportiva do Iate Clube do Rio de Janeiro, a qual é comercializada na sua própria peixaria, devido à apreciação de sua carne. Contudo a presença de helmintos, inclusive na musculatura, resulta em perdas comerciais devido ao seu aspecto repugnante. O objetivo desta investigação foi identificar taxonomicamente estes helmintos utilizando dados de análises morfométricas e morfológicas através das microscopias ótica e eletrônica de varredura e determinar sua significância higiênico-sanitária. Em janeiro e novembro de 2014, sete espécimes de C. hippurus foram necropsiados e seus órgãos investigados. Os helmintos encontrados foram identificados como plerocercoides de Tentacularia coryphaenae, um cestoide Trypanorhyncha. Os sete espécimes de C. hippurus estavam parasitados por um total de 204 plerocercoides, tendo como os sítios de infecção a musculatura, mesentério, estômago e serosa do fígado. Além da repugnância destes parasitos, a presença de plerocercoides é um fator preocupante porque há o risco de reações alérgicas em humanos, por isto salienta a sua significância higiênico-sanitária no monitoramento destes parasitos.Palavras-chave: Cestoide; Trypanorhyncha; dourado; higiene do pescado; pesca esportiva.

ABSTRACTCoryphaena hippurus, or dolphinfish, is a popular species of fish pursued by sport fishing tournaments of the Yacht Club of Rio de Janeiro, wich markets then in its own fish market, because of its desirable flesh. However, the presence of helminths, including in the musculature, results in commercial losses due their repugnant appearance. The aim of this investigation was to identify taxonomically these helminthes using morphometrical and morphological data from analyses using optical and scanning electron microscopy, and to determine their hygienic-sanitary significance. Seven specimens of C. hippurus collected in January and November 2014 were necropsied and had their organs investigated. The helminths encountered included plerocercoids of Tentacularia coryphaenae, a trypanorhynch cestode. The seven specimens of C. hippurus were parasitized by a total of 204 plerocercoids, with infection sites being musculature, mesentery, stomach and liver serosa. Beyond the repugnance of these parasites, the presence of plerocercoids is worrisome because of the potential risk of allergic reactions by humans, thereby reinforcing the hygienic-sanitary significance of monitoring for these parasites.Key words: Cestode; Trypanorhyncha; dolphinfish; fish hygiene; sport fishing.

B. Inst. Pesca, São Paulo, 43(2): 266 - 273, 2017

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INTRODUCTION

The Yacht Club of Rio de Janeiro (ICRJ), sponsors sport fishing tournaments during which several species of oceanic fish are captured. These fish include economically valuable species with desirable meat, and so they are not only considered trophies, but are also sent to ICRJ’s own fish market. One of these species is the dolphinfish, Coryphaena hippurus Linneaus, 1758. The species C. hippurus is cosmopolitan, which has a cosmopolitan distribution throughout, tropical and subtropical seas (GIBBS and COLLETTE, 1959; MENEZES and FIGUEIREDO, 1980). In Brazil, the dolphinfish is highly valued for food and is an important constituent of recreational and commercial fisheries (GIBBS and COLLETTE, 1959; DITTY et al., 1994; PALOMINO et al., 1998).

The maintenance of hygienic-sanitary conditions at the ICRJ fish market has been a concern. For example, larvae of trypanorhynch cestodes have been found in the musculature of dolphinfish at the ICRJ fish market, which usually produce a repugnant appearance resulting losses in sales. Cestodes of the order Trypanorhyncha possess worldwide distribution, and occur in marine animals of tropical and subtropical regions (PALM, 2004).

As adul t s these ces todes inhabi t the gastrointestinal tract of elasmobranchs, while their larval forms are found in several species of teleost and elasmobranch fish, and a variety of marine invertebrates (CAMPBELL and BEVERIDGE, 1994). According to the Brazilian legislation that deals with fish and their derivative products, any fish with a repugnant appearance is considered improper for consumption, as in any musculature possessing massive parasite infection, whether or not it may affect the health of consumers (BRASIL, 2007). Furthermore, the presence of trypanorhynch larvae in fish is considered disconcerting since they can pose a risk of allergic reactions in humans (MATTOS et al., 2013).

The aims of this investigation were to: (1) identify the species of trypanorhynch cestodes parasitizing C. hippurus caught during sport fishing tournaments in the state of Rio de Janeiro by means of morphological and morphometric analyses using optical and scanning electron microscopy of specimens retrieved from the site of infection; (2) demonstrate the hygienic-sanitary significance of these parasites to collective human health; and (3) provide baseline data for subsequent investigations.

METHODS

In January and November 2014, seven specimens of dolphinfish, C. hippurus (85-100 cm total length and 6.5-7 kg) caught by fishermen during ocean sport fishing of the coast of the municipality of Cabo Frio, state of Rio de Janeiro, Brazil were brought to ICRJ and sent to its fish market. Fish species were identified according to MENEZES and FIGUEIREDO (1980).

The fish were then necropsied and filleted, and their organs separated into plastic bags, labeled and transported on ice in isothermic boxes for examination in the Laboratory of Helminth Parasites of Vertebrates, Oswaldo Cruz Institute, Oswaldo Cruz Foundation (FIOCRUZ), Rio de Janeiro. The three dolphinfish captured in January 2014 possessed plerocercoids of trypanorhynch cestodes parasitizing musculature, stomach, liver serosa and mesentery. The other four dolphinfish, caught in November 2014, had only their musculature examined, because their commercialization was prohibited by the massive presence of trypanorhynch plerocercoids.

In the laboratory, retrieved cestodes were placed in Petri dishes containing destiled water and maintained in a refrigerator for at least 24h to permit the relaxation of scolices and extrovertion tentacles. Some of the larvae were fixed in cold AFA, stained with Langeron’s carmine, differentiated in 0.5% hydrochloric acid-ethanol solution, dehydrated in a series of increasing alcohol concentrations and clarified with beach-wood creosote. Ten specimens were then mounted whole preserved in Canada balsam and measured, while the other specimens were preserved in 70ºGL ethanol (KNOFF and GOMES, 2012).

The specimens were observed with an Olympus BX-41 bright-field microscope, and images were obtained using a Cannon Power Shot A640 digital camera coupled to Zeiss Axiophot microscope. Topographical descriptions of surface of scolices was performed using scanning electron microcopy (SEM). For SEM the cestodes were processed as described by LOPES TORRES et al. (2013), which envolved, in short, fixation in ethanol 70ºGL, dehydration in an acetone series, CO2 critical-point drying and gold coating (20 nm deposition). Images were made using a JEOL LV 6940 SEM under 30kV acceleration voltage.

Taxonomic identification followed CAMPBELL and BEVERIDGE (1994), BEVERIDGE and

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CAMPBELL (1996), PALM (2000, 2004) and KNOFF et al. (2004). Terminology for cestode larvae followed CHERVY (2002). Measurements are given in millimeters and as range followed by means in parenthesis. For confirmation of identification, specimens were compared with the plerocercoids of T. coryphaenae collected from individuals of Genypterus brasiliensis from Rio de Janeiro, RJ, Brazil (CHIOC no. 36420); Scomberomorus cavala from Rio de Janeiro, RJ, Brazil (CHIOC no. 35633); Lophius gastrophysus from Niterói, RJ, Brazil (CHIOC no. 36691); Katsuwonus pelamis from RJ, Brazil (CHIOC no. 36541 a-b), and Cabo Frio, RJ, Brazil (CHIOC no. 37150 a-b, 37151, 37152); and Thunus albacares from Cabo Frio, RJ, Brazil (CHIOC 37153).

Voucher specimens were deposited in the Hel-minthological Collection of the Oswaldo Cruz Insti-tute (CHIOC), FIOCRUZ, Rio de Janeiro, RJ, Brazil.

RESULTS

The three specimens of C. hippurus collected in January 2014 were parasitized by a total of 108 plerocercoids of trypanorhynch cestodes in the abdominal musculature, mesentery, stomach and liver serosa. The four hosts collected in November 2014 were parasitized by a total of 96 plerocercoids

of the same species. These fish were removed from commercialization and discarded by the ICRJ fish market due to the massive infections in the abdominal musculature and the severe hemorrhage caused by the large number of cestodes (Figure 1 a-c). All plerocercoids were found alive and demonstrated high motility.

CestodaTrypanorhyncha Diesing, 1863Tentaculariidae Poche,1926Tentacularia Bosc,1797Tentacularia coryphaenae Bosc, 1797 (Figures 2 a-b; 3 a-c)Description: based on 10 mounted and measured,

not compressed specimens, and 9 SEM specimens. Scolex acraspedote, 3.75-7.08 (4.80) (n=10) long with velum included, widest at the level of anterior portion of pars bothrialis or velum, 1.20-1.83 (1.46) (n=10) wide. Pars bothrialis with elongated bothriae, occupying almost 80% of the scolex, with sessile margins, 2.25-6.50 (3.83) (n=6) long, 1.20-1.65 (1.42) (n=6) wide. Pars vaginalis nearly 4.5 times smaller than scolex, with straight sheaths on its anterior two-thirds and sinuously close to the bulbs, 0.78-1.28 (0.98) (n=8) long. Pars bulbosa, 0.88-1.15 (1.02) (n=8) long, 0.20-0.53 (0.37) (n=8) wide. Individual bulbs, 0.75-1.08 (0.86) (n=27) long, 0.10-0.25 (0.15) (n=27) wide. Pars post-bulbosa well-developed. Velum, 0.68-1.75 (1.17) (n=10) long.

Figure 1. Tentacularia coryphaenae plerocercoid infection in Coryphaena hippurus. a. Fillets of the abdominal musculature of hosts collected in January 2014; arrows indicate the presence of the cestode parasites. b-c. Musculature of hosts collected in November 2014; arrows indicate the large number of cestodes causing severe hemorrhage. Bars a = 2.5 cm; b-c = 3 cm.



Appendix 0.98-6.15 (2.07) long. Tegumentary structures present include porosities and filiform microtriches on the scolex, and hook-like microtriches along the bothrial margins.

Width of tentacles, without hooks, 0.07-0.09 (0.08) (n=35) at basal region and, 0.05-0.07 (0.06) (n=35), at metabasal region. Basal hooks tridentiforme 0.008-0.013 (0.009) (n=30) long, implantation basal, 0.006-0.012 (0.009) (n=30) wide. Basal armature of tentacles with bilateral symmetry of ascending hook rows with identical V-shaped patterns on bothrial and antibothrial surfaces, and forming an identical,

inverted, unarmed V-shaped pattern, on the external and internal surfaces. Metabasal armature with rotational symmetry, arranged in quincunx. Metabasal hooks unciforme 0.025-0.033 (0.027) long, base 0.020-0.030 (0.024) wide. Number of hooks/row 9-10. Hooks of same shape on both sides of tentacle.

Taxonomic summaryCollected specimens: 204 plerocercoids. Specimens deposited: plerocercoids CHIOC no.

37998 a-e.Host: C. hippurus.Locality: latitude 21º23’ S, longitude 41º45’ W, Cabo Frio, RJ, Brazil.

Figure 2. Tentacularia coryphaenae plerocercoid in Coryphaena hippurus under bright-field microscopy. a. Entire worm, showing tentacles (T), pars bothrialis (Bo), pars vaginalis (Pv), pars bulbosa (Pb), pars post-bulbosa (Ppb), velum (V), and appendix (Ap). b. Detail of extroverted tentacles, indicating the regions of basal armature (BA) and metabasal armature (MA), on the bothrial surface. Bars a = 1000 µm; b = 100 µm.

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Figure 3. Tentacularia coryphaenae plerocercoid in Coryphaena hippurus under scanning electron microscopy. a. Detail of anterior region of scolex, showing tentacles and bothrial region. b. Detail of basal region in bilateral symmetry, with internal (I) and external surfaces (E) showing an unarmed inverted V-shaped pattern, and the bothrial surface (B) showing ascending rows of hooks (trident-like) in a V-shaped pattern beginning in the metabasal region. c. Detail of the metabasal region with uncinate hooks with rotational symmetry and a quincunxial arrangement on the bothrial surface. Bars a = 200 µm; b = 50 µm; c = 20 µm.

DISCUSSION

The specimens of T. coryphaenae collected in the present study are in accordance with the descriptions of DOLLFUS (1942), KNOFF et al. (2004) and PALM (2004). The patterns of basal and metabasal hooks of the tentacular armature agree with those observed by BEVERIDGE and CAMPBELL (1996), PALM (2000) and KNOFF et al. (2004). In the present study, the presence of tegumentary ultrastructures of the scolex, such as porosities, filiform microtriche, and hook-like microtriches along the bothrial margins, were also observed by BILQEES and KHURSHID (1988), PALM (1995, 2000, 2004) and KNOFF et al. (2004).

In Brazil, T. coryphaenae has been reported parasitizing a variety of marine teleost hosts, including the dolphinfish and elasmobranch fishes. All these teleosteans were collected from the coastal waters of the state of Rio de Janeiro. SILVA and SÃO CLEMENTE (2001) examined 596 fillets from 41 individuals of C. hippurus (size range of 65-148 cm total length) from the same area and found T. coryphaenae present in 25 fillets; 1 infected fillet from the 65-106 cm size class, and 24 infected fillets from the 107-148 cm size class.

A total of 56 parasites were found, for a prevalence of 0.47% and an intensity of infection of 1 parasite per fillet in the smaller size class, and a prevalence of 6.25% and an intensity of infection of 2.29 parasites per fillet in the larger size class; however, the authors did not provide information about the number of parasitized fish and the mean intensity of infection, Moreover, SÃO CLEMENTE (personal information)

did not observe massive infections by this species in the musculature.

Tentacularia coryphaenae has been reported from the mesentery of Genypterus brasiliensis with a prevalence of 1.35 and an intensity of 1 specimen per individual (SÃO CLEMENTE et al., 2004); in Katsuwonus pelamis L., 1758, with a prevalence of 92.9% and mean intensity of 36.3 and a range of infection of 1-110 plerocercoids per fish in the abdominal and body musculature (AMATO et al., 1990), and in another case with a prevalence of 66.7%, mean intensity of 5.8 and range of infection of 1-17 parasites in the musculature (ALVES and LUQUE, 2006); in Lophius gastrophysus Miranda-Ribeiro, 1915, with a prevalence of 2.3% and an intensity of 1 parasite in the musculature (SÃO CLEMENTE et al., 2007); in Scomberomorus cavalla (Cuvier, 1829), with a prevalence of 3% and an intensity of 2 parasites in the mesentery (DIAS et al., 2011).

Among elasmobranchs, T. coryphaenae has been reported parasitizing species off the coast of a variety of different Brazilian states, including being found in the stomach and spiral valve of a Carcharinus longimanus Poey, 1861, in Recife, state of Pernambuco, without information about the number of parasites collected (REGO, 1977), and from the spiral valve of Prionace glauca (L., 1758), C. longimanus and C. obscurus (Lesueur, 1818) collected in the state of Santa Catarina with prevalences of 16.7%, 50% and 100% and mean intensities of 0.2, 0.5 and 12 parasites per fish, respectively (KNOFF et al., 2002, 2004). Comparing the data of the present study with data for teleost species of commercial importance studied



along the Brazilian coast, the specimens of C. hippurus studied herein (the previous report of C. hippurus did not make mention of a massive infection) and K. pelamis had highest indices of parasitism. The finding may be due to the influence of different physico-chemical factors and biological interactions experienced by the fish parasite communities of the different environments.

The species T. coryphaenae is known to exhibit low host specificity during its final and intermediate hosts. It is distributed worldwide in tropical and subtropical seas, and inhabit widely migrating scombroids and large pelagic predatory fish as second intermediate hosts. Adults of T. coryphaenae have been recorded from 11 different final host species, and is known from over 80 species of smaller and larger pelagic or oceanic fish and squids (PALM, 2004).

The findings of the present study corroborate previous reports and CHIOC examined material that the dolphinfish C. equiselis and C. hippurus, and tunas K. pelamis and T. albacares, as well as other pelagic and cosmopolitan migratory teleosts known are intermediate hosts in Brazil and throughout the world, and reinforce the hypothesis that these fish are acting as bridges for transfer of T. coryphaenae throughout marine food webs and among oceans (PALM et al., 2007).

Hepatoxylon trichiuri (Holten, 1802) Bosc, 1811, is another trypanorhynch species that parasitizes C. hippurus in Brazil (SÃO CLEMENTE et al., 2001), with a prevalence of 4.9% and a mean intensity of 1 parasite per fish in the liver and stomach serosas, however, none of the fish of the present study were parasitized with this species.

AMATO et al. (1990) suggested the removal of abdominal musculature as method for exporting K. pelamis free of these trypanorhynch metacestodes, however, this procedure does not seem viable in the present study, because, of widespread distribution of large numbers of metacestodes in muscular fascia. This observation was also reported for another trypanorhynch species, Myxonybelinia sp., a parasite of Lophius gastrophysus Miranda-Ribeiro, 1915, collected off the coast of the state of Rio de Janeiro (SÃO CLEMENTE et al. , 2007). The present study represents the first report of T. coryphaenae causing severe hemorrhage in C. hippurus, which has never even been referred to in previous studies (SILVA and SÃO CLEMENTE, 2001).

CONCLUSIONS

The present study found T. coryphaenae plerocercoids to have significant hygienic-sanitary imporytance for C. hippurus, mainly because of its massive presence in the musculature and the resulting severe hemorrhage. These findings indicate that commerce with this fish species is impracticable in the ICRJ fishmarket due to the repugnant appearance of parasitized individuals.

The possibility of causing hypersensitivity reactions in humans illustrates the importance of inspecting fish for these trypanorhynch parasites. Furthermore, the results of this study suggest that in the future immunological studies, with a murine model, into these plerocercoids will be subject are needed for evaluating the risk of causing allergic reactions in humans.

ACKNOWLEDGMENTS

The authors would like to thank the Yacht Club of Rio de Janeiro (ICRJ) for the donation of the study fish; Paula Breves Boghossian, who kindly made contact with fishermen and the fishmongers of ICRJ where the fish were acquired; to Dr. Sérgio Henrique Seabra (Laboratório de Tecnologia em Bioquímica e Microscopia, Universidade Estadual da Zona Oeste, Rio de Janeiro) for conducting the scanning electronic microscopy; to Heloísa Nogueira Diniz and Ricardo Baptista Schmidt (Serviço de Produção e Tratamento de Imagens do Instituto Oswaldo Cruz, Fiocruz) for processing the figures; and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for partial financial support.

REFERENCES

ALVES, D.R.; LUQUE, J.L. 2006 Community ecology of the metazoan parasites of five Scombrids species (Perciformes: Scombridae), from the coastal zone of the State of Rio de Janeiro, Brazil. Revista Brasileira de Parasitologia Veterinária, 15 (4): 167-181.

AMATO, J.F.R.; SÃO CLEMENTE, S.C.; OLIVEIRA, G.A. 1990 Tentacularia coryphaenae Bosc, 1801 (Eucestoda: Trypanorhyncha) in the inspection

SILVA et al.


272

and technology of the Skipjack Tuna, Katsuwonus pelamis (L.) (Pisces: Scombridae). Atlântica, 12 (1): 73-77.

BEVERIGDE, I.; CAMPBELL, R.A. 1996 New records and descriptions of trypanorhynch cestodes from Australian fishes. Records of the South Australian Museum, 29 (1): 1-22.

BILQEES, F. M.; KHURSHID, N. 1988 Surface ultrastructure of Tentcularia coryphaenae Bosc, 1797 (Cestoda: Trypanorhyncha) from the fish Cybium guttatum of Karachi coast. Proceedings of the Parasitology, 5(1): 1-5.

BRASIL, 2007 Ministério da Agricultura, Pecuária e Abastecimento. Decreto nº 30.691, de 29 de março de 1952. Aprova o novo Regulamento da Inspeção Industrial e Sanitária de Produtos de Origem Animal. Diário Oficial da União, Brasília, DF, 7 julho de 1952, Seção 1: 10785.

CAMPBELL, R.A.; BEVERIGDE, I. 1994 Order Trypanorhyncha Diesing, 1863. In: KHALIL, L.F.; JONES, A.; BRAY, R.A. Keys to the Cestode Parasites of Vertebrates. St. Albans, CAB International. p. 51-148.

CHERVY, L. 2002 The terminology of larval cestodes or metacestodes. Systematic Parasitology, 52(1): 1-33.

DIAS, F.J.E.; SÃO CLEMENTE, S.C.; PINTO, R.M.; KNOFF, M. 2011 Anisakidae nematodes and Trypanorhyncha cestodes of hygienic importance infecting the king mackerel Scomberomorus cavalla (Osteichthyes: Scombridae) in Brazil. Veterinary Parasitology, 175(3-4): 351- 355.

DITTY, J.G.; SHAW, R.F; GRIMES, C.B.; COPE, J.S. 1994 Larval development, distribution, and abundance of commom dolphin, Coryphaena hippurus, and C. esquiselis (Family: Coryphaenidae), in the northern Gulf of Mexico. Fishery Bulletin, 92(2): 275-291.

DOLLFUS, R.P. 1942 Études critiques sur les Tétrarhynches du Museúm de Paris. Archives du Museum D’Histoire Naturelle, 19(1): 1-467.

GIBBS, R.H.; COLLETTE, B.B. 1959 On the

identification, distribution and biology of the dolphins, Coryphaena hippurus and C. equiselis. Bulletin of Marine Science of the Gulf and Caribbean, 9(2): 117-152.

KNOFF, M.; GOMES, D.C. 2012 Capítulo 3. M e t o t o d o l o g i a b á s i c a p a r a c o l e t a e processamento de helmintos parasitos. In: MOLINARO, E.; CAPUTO, L.; AMENDOEIRA, R. Conceitos e Métodos para formação de profissionais em laboratórios de saúde: volume 5. Ed. Escola Politécnica de Saúde Joaquim Venâncio, Fundação Oswaldo Cruz, Rio de Janeiro. p. 251-281.

KNOFF, M.; SÃO CLEMENTE, S.C.; PINTO, R.M.; GOMES, D.C. 2002 Prevalência e intensidade de infecção de cestóides Trypanorhyncha elasmobrânquios nos Estados Paraná e Santa Catarina, Brasil. Parasitologia Latinoamericana, 57(3-4): 149-157.

KNOFF, M.; SÃO CLEMENTE, S.C.; PINTO, R.M.; LANFREDI, R.M.; GOMES, D.C. 2004 New records and expanded descriptions of Tentacularia coryphaenae and Hepatoxylon trichiuri homeacanth trypanorhynchs (Eucestoda) from Carcharhinid sharks from the State of Santa Catarina off-shore, Brazil. Revista Brasileira de Parasitologia Veterinária, 13(2): 73-80.

LOPES TORRES, E.J.; SOUZA, W.; MIRANDA, K. 2013 Comparative analysis of Trichuris muris surface using conventional, low vacuum, environmental and field emission scanning electron microscopy. Veterinary Parasitology, 196(3-4): 409-416.

MATTOS, D.P.B.G; VERÍCIMO, M.A.; SÃO CLEMENTE, S.C. 2013 O Pescado e os Cestoides Trypanorhyncha – Do Aspecto Higiênico ao potencial alergênico. Veterinária Notícias, 19(2): 127-139.

MENEZES, N.A.; FIGUEIREDO, J.L. 1980 Manual de Peixes Marinhos do Sudeste do Brasil. IV. Teleostei (3). São Paulo: Universidade de São Paulo, Museu de Zoologia. 96 p.

PALM, H.W. 1995 Berichte aus den Institute für Meereskunde Kiel an der Christian-Albrechts-



Universität Kiel. Nr. 275. Untersuchungen zur Systematik von Rüsselbandwürmern (Cestoda: Trypanorhyncha) aus atlantischen Fischen. Kiel: Institut für Meereskunde an der Universität Kiel, Bibliothek, 238 p.

PALM, H.W. 2000 Trypanorhynch cestodes from Indonesian coastal waters (East Indian Ocean). Folia Parasitologica, 47(2): 123-134.

PALM, H.W. 2004 The Trypanorhyncha Diesing, 1863. Bogor: PKSPL-IPB Press. 710 p.

PALM, H.W.; WAESCHENBACH, A.; LITTLEWOOD, D.T.J. 2007 Genetic diversity in the trypanorhynch cestode Tentacularia coryphaenae Bosc, 1797: evidence for a cosmopolitan distribution and low host specificity in the teleost intermediate host. Parasitology Research, 101(1): 153-159.

PALOMINO, B.A.; MAGAÑA, F.G.; CÁRDENAS, L.A.A.; MELLO, A.F.M.; ROMERO, J.R. 1998 Aspectos alimentarios del dorado Coryphaena hippurus Linnaeus, 1758 en Cabo San Lucas, baja California sur, Mexico. Ciencias Marinas, 24(3): 253-265.

REGO, A.A. 1977 Cestoides parasitas de Carcharinus longimanus Poey, 1861. Revista Brasileira de Biologia, 37(4): 847-852.

SÃO CLEMENTE, S.C.; PEREIRA JR., J.; KNOFF, M.; SILVA, C.M.; FERNANDEZ, J.G.; COUSIN, J.C. 2001 Hepatoxylon trichiuri (Holten, 1802) Dollfus, 1942, Hepatoxylidae Dollfus, 1940 (Eucestoda: Trypanorhyncha) em Prionace glauca (Linnaeus, 1758), do litoral do estado do Rio Grande do Sul e em Coryphaena hippurus Linnaeus, 1758, do litoral do estado do Rio de Janeiro, Brasil. Parasitología al Día, 25(..): 135-137.

SÃO CLEMENTE, S.C.; KNOFF, M.; PADOVANI, R.E.S.; LIMA, F.C.; GOMES, D.C. 2004 Cestóides Trypanhorhyncha parasitos de congro-rosa, Genypterus brasiliensis, Regan,1903 comercializados nos municípios de Niterói e rio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veterinária, 13(3): 97-102.

SÃO CLEMENTE, S.C.; KNOFF, M.; LIMA, F.C.; ANDRADA, C.G.; FELIZARDO, N.N.;

PADOVANI, R.E.S.; GOMES, D.C. 2007 Cestóides Trypanorhyncha parasitos de peixe sapo-pescador, Lophius gastrophysus Miranda-Ribeiro, 1915 comercializados no Estado do Rio de Janeiro. Revista Brasileira de Parasitologia Veterinária, 16(1): 37-42.

SILVA, C.M.; SÃO CLEMENTE, S.C. 2001 Nematoides da família Anisakidae e cestóides da Ordem Trypanorhyncha em filés de dourado (Coryphaena hippurus) e ariocó (Lutjanus synagris) e sua importância na inspeção de pescado. Higiene Alimentar, 15(80-81): 75-79.

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